Contrasting behavior of heterochromatic and euchromatic chromosome portions and pericentric genome separation in pre-bouquet spermatocytes of hybrid mice

Abstract

The spatial distribution of parental genomes has attracted much interest because intranuclear chromosome distribution can modulate the transcriptome of cells and influence the efficacy of meiotic homologue pairing. Pairing of parental chromosomes is imperative to sexual reproduction as it translates into homologue segregation and genome haploidization to counteract the genome doubling at fertilization. Differential FISH tagging of parental pericentromeric genome portions and specific painting of euchromatic chromosome arms in Mus musculus (MMU) × Mus spretus (MSP) hybrid spermatogenesis disclosed a phase of homotypic non-homologous pericentromere clustering that led to parental pericentric genome separation from the pre-leptoteneup to zygotene stages. Preferential clustering of MMU pericentromeres correlated with particular enrichment of epigenetic marks (H3K9me3), HP1-γ and structural maintenance of chromosomes SMC6 complex proteins at the MMU major satellite DNA repeats. In contrast to the separation of heterochromatic pericentric genome portions, the euchromatic arms of homeologous chromosomes showed considerable presynaptic pairing already during leptotene stage of all mice investigated. Pericentric genome separation was eventually disbanded by telomere clustering that concentrated both parental pericentric genome portions in a limited nuclear sector of the bouquet nucleus. Our data disclose the differential behavior of pericentromeric heterochromatin and the euchromatic portions of the parental genomes during homologue search. Homotypic pericentromere clustering early in prophase I may contribute to the exclusion of large repetitive DNA domains from homology search, while the telomere bouquet congregates and registers spatially separated portions of the genome to fuel synapsis initiation and high levels of homologue pairing, thus contributing to the fidelity of meiosis and reproduction.Electronic supplementary materialThe online version of this article (doi:10.1007/s00412-014-0479-4) contains supplementary material, which is available to authorized users.

Modulation of Prdm9-controlled meiotic chromosome asynapsis overrides hybrid sterility in mice

“…In spite of the known role of subtelomeric (bouquet) association in chromosome pairing ( Ishiguro et al, 2014 ; Scherthan et al, 2014 ), the location of the consubspecific sequence at the telomeric end was not essential for synapsis (p=0.9573, F-test). The PWD/PWD intervals of sufficient size rescued synapsis whether located at the centromeric (proximal, n = 14 cases), interstitial (n = 3), or telomeric (distal, n = 14) position ( Figure 3—source data 1 – 6 ).…”

Attenuated chromatin compartmentalization in meiosis and its maturation in sperm development

“…3b). Studies utilizing microscopy demonstrated that, during meiotic prophase, both chromosome ends attach to the nuclear membrane 25 and, in particular, the acrocentric ends tend to associate because of the frequent association of pericentromeric heterochromatin 26 . Our Hi-C results are consistent with these microscopic observations.…”

Meiotic chromosome mobility in fission yeast is resistant to environmental stress

“…Meiotic homology search in many organisms is associated with chromosome movements in the presence of physiological DSBs 12 13 14 15 . In the asynaptic meiosis of the fission yeast Schizosaccharomyces pombe a synaptonemal complex is absent but chromosomes are aligned by oscillating nuclear mobility driven by the astral microtubule-bound spindle pole body (SPB) to which telomeres are attached, giving rise to the so-called horsetail nucleus throughout much of prophase I 7 16 .…”